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Title (Primary) Algal remodeling in a ubiquitous planktonic photosymbiosis
Author Decelle, J.; Stryhanyuk, H.; Gallet, B.; Veronesi, G.; Schmidt, M.; Balzano, S.; Marro, S.; Uwizeye, C.; Jouneau, P.-H.; Lupette, J.; Jouhet, J.; Maillot-Maréchal, E.; Schwab, Y.; Schieber, N.L.; Tucoulou, R.; Richnow, H.; Finazzi, G.; Musat, N.;
Journal Current Biology
Year 2019
Department ISOBIO;
Volume 29
Issue 6
Language englisch;
POF III (all) T41;
Keywords symbiosis; plankton; microalga; single-cell imaging; photosynthesis; mass spectrometry imaging; 3D electron microscopy; eukaryotes; plastid; Phaeocystis
Abstract Photosymbiosis between single-celled hosts and microalgae is common in oceanic plankton, especially in oligotrophic surface waters. However, the functioning of this ecologically important cell-cell interaction and the subcellular mechanisms allowing the host to accommodate and benefit from its microalgae remain enigmatic. Here, using a combination of quantitative single-cell structural and chemical imaging techniques (FIB-SEM, nanoSIMS, Synchrotron X-ray fluorescence), we show that the structural organization, physiology, and trophic status of the algal symbionts (the haptophyte Phaeocystis) significantly change within their acantharian hosts compared to their free-living phase in culture. In symbiosis, algal cell division is blocked, photosynthesis is enhanced, and cell volume is increased by up to 10-fold with a higher number of plastids (from 2 to up to 30) and thylakoid membranes. The multiplication of plastids can lead to a 38-fold increase of the total plastid volume in a cell. Subcellular mapping of nutrients (nitrogen and phosphorous) and their stoichiometric ratios shows that symbiotic algae are impoverished in phosphorous and suggests a higher investment in energy-acquisition machinery rather than in growth. Nanoscale imaging also showed that the host supplies a substantial amount of trace metals (e.g., iron and cobalt), which are stored in algal vacuoles at high concentrations (up to 660 ppm). Sulfur mapping reveals a high concentration in algal vacuoles that may be a source of antioxidant molecules. Overall, this study unveils an unprecedented morphological and metabolic transformation of microalgae following their integration into a host, and it suggests that this widespread symbiosis is a farming strategy wherein the host engulfs and exploits microalgae.
ID 21716
Persistent UFZ Identifier
Decelle, J., Stryhanyuk, H., Gallet, B., Veronesi, G., Schmidt, M., Balzano, S., Marro, S., Uwizeye, C., Jouneau, P.-H., Lupette, J., Jouhet, J., Maillot-Maréchal, E., Schwab, Y., Schieber, N.L., Tucoulou, R., Richnow, H., Finazzi, G., Musat, N. (2019):
Algal remodeling in a ubiquitous planktonic photosymbiosis
Curr. Biol. 29 (6), 968 - 978.e4